Hiding in the heterochromatin: Endogenous pararetroviruses escape elimination from the genome of sugar beet (Beta vulgaris)

Endogenous pararetroviruses (EPRVs) are a widespread component of plant genomes. They can persist through millions of years without affecting their plant hosts due to a loss of activity. However, in some cases, these ancient viral sequences can be activated through reverse transcription, thus forming virulescent counterparts that are associated with devastating diseases. Our genome-wide screen showed that there are three host-specific EPRV families (beetEPRVs) in the genome of the crop sugar beet (Beta vulgaris). Using next-generation sequence reads and assemblies, we reconstructed full-length in silico representatives for each family. We found heterogeneous element features, e.g. regarding the arrangement of protein domains within the EPRV element, the degree of fragmentation, and a preference for different sequence contexts. Nevertheless, all beetEPRV families can be assigned to the genus Florendovirus within the family Caulimoviridae. We observed several small RNAs that target beetEPRVs in a family-specific manner, indicating that these integrated viruses are silenced through RNA degradation and RNA-dependent DNA methylation.Focusing on canonical family beetEPRV3, we investigated its occurrence, distribution and abundance by fluorescent in situ and Southern hybridisation. We detected beetEPRV3 spread to all 18 sugar beet chromosomes, occurring preferentially in clusters and without exclusion of the centromeres. Variants of this viral sequence also exist in the genomes of related wild species, assuming that the initial beetEPRV3 infection took place 13.4 to 7.2 million years ago. Our study in beet exemplarily illustrates possible long-term scenarios for a plant after an EPRV infection, including fixation, genomic amplification, and containment of EPRV virulence.